Prognostication in the early stage of traumatic coma is a common challenge in the neuro-intensive care unit. We report the unexpected recovery of functional milestones (i.e., consciousness, communication, and community reintegration) in a 19-year-old man who sustained a severe traumatic brain injury. The early magnetic resonance imaging (MRI) findings, at the time, suggested a poor prognosis.
During the first year of the patient’s recovery, MRI with diffusion tensor imaging and T2*-weighted imaging was performed on day 8 (coma), day 44 (minimally conscious state), day 198 (post-traumatic confusional state), and day 366 (community reintegration). Mean apparent diffusion coefficient (ADC) and fractional anisotropy values in the corpus callosum, cerebral hemispheric white matter, and thalamus were compared with clinical assessments using the Disability Rating Scale (DRS).
Extensive diffusion restriction in the corpus callosum and bihemispheric white matter was observed on day 8, with ADC values in a range typically associated with neurotoxic injury (230–400 × 10−6 mm2/s). T2*-weighted MRI revealed widespread hemorrhagic axonal injury in the cerebral hemispheres, corpus callosum, and brainstem. Despite the presence of severe axonal injury on early MRI, the patient regained the ability to communicate and perform activities of daily living independently at 1 year post-injury (DRS = 8).
MRI data should be interpreted with caution when prognosticating for patients in traumatic coma. Recovery of consciousness and community reintegration are possible even when extensive traumatic axonal injury is demonstrated by early MRI.
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Ling GS, Marshall SA. Management of traumatic brain injury in the intensive care unit. Neurol Clin. 2008;26:409–26, viii.
Langlois JA, Rutland-Brown W, Thomas KE. Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Atlanta: N.C.F.I.P. Centers for Disease Control and Prevention; 2006.
Selassie AW, Zaloshnja E, Langlois JA, et al. Incidence of long-term disability following traumatic brain injury hospitalization, United States, 2003. J Head Trauma Rehabil. 2008;23:123–31.
Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet. 1972;1:734–7.
Giacino JT, Ashwal S, Childs N, et al. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58:349–53.
Katz DI, Polyak M, Coughlan D, et al. Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1–4 year follow-up. Prog Brain Res. 2009;177:73–88.
Skandsen T, Kvistad KA, Solheim O, et al. Prognostic value of magnetic resonance imaging in moderate and severe head injury: a prospective study of early MRI findings and one-year outcome. J Neurotrauma. 2011;28:691–9.
Gennarelli TA, Spielman GM, Langfitt TW, et al. Influence of the type of intracranial lesion on outcome from severe head injury. J Neurosurg. 1982;56:26–32.
Bell RS, Vo AH, Neal CJ, et al. Military traumatic brain and spinal column injury: a 5-year study of the impact blast and other military grade weaponry on the central nervous system. J Trauma. 2009;66:S104–11.
Estraneo A, Moretta P, Loreto V, et al. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology. 2010;75:239–45.
Voss HU, Uluc AM, Dyke JP, et al. Possible axonal regrowth in late recovery from the minimally conscious state. J Clin Invest. 2006;116:2005–11.
Luaute J, Maucort-Boulch D, Tell L, et al. Long-term outcomes of chronic minimally conscious and vegetative states. Neurology. 2010;75:246–52.
Nakase-Richardson R, Whyte J, Giacino JT, et al. Longitudinal outcome of patients with disordered consciousness in the NIDRR TBI Model Systems Programs. J Neurotrauma. 2012;29:59–65.
Lammi MH, Smith VH, Tate RL, Taylor CM. The minimally conscious state and recovery potential: a follow-up study 2 to 5 years after traumatic brain injury. Arch Phys Med Rehabil. 2005;86:746–54.
Maas AI, Steyerberg EW, Butcher I, et al. Prognostic value of computerized tomography scan characteristics in traumatic brain injury: results from the IMPACT study. J Neurotrauma. 2007;24:303–14.
Steyerberg EW, Mushkudiani N, Perel P, et al. Predicting outcome after traumatic brain injury: development and international validation of prognostic scores based on admission characteristics. PLoS Med. 2008;5:e165.
Murray GD, Butcher I, McHugh GS, et al. Multivariable prognostic analysis in traumatic brain injury: results from the IMPACT study. J Neurotrauma. 2007;24:329–37.
Perel P, Arango M, Clayton T, et al. Predicting outcome after traumatic brain injury: practical prognostic models based on large cohort of international patients. BMJ. 2008;336:425–9.
Lagares A, Ramos A, Perez-Nunez A, et al. The role of MR imaging in assessing prognosis after severe and moderate head injury. Acta Neurochir (Wien). 2009;151:341–56.
Firsching R, Woischneck D, Diedrich M, et al. Early magnetic resonance imaging of brainstem lesions after severe head injury. J Neurosurg. 1998;89:707–12.
Gentry LR, Godersky JC, Thompson B, Dunn VD. Prospective comparative study of intermediate-field MR and CT in the evaluation of closed head trauma. AJR Am J Roentgenol. 1988;150:673–82.
Paterakis K, Karantanas AH, Komnos A, Volikas Z. Outcome of patients with diffuse axonal injury: the significance and prognostic value of MRI in the acute phase. J Trauma. 2000;49:1071–5.
Gentry LR, Godersky JC, Thompson BH. Traumatic brain stem injury: MR imaging. Radiology. 1989;171:177–87.
Gentry LR. Imaging of closed head injury. Radiology. 1994;191:1–17.
Adams JH, Doyle D, Ford I, et al. Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology. 1989;15:49–59.
Kampfl A, Schmutzhard E, Franz G, et al. Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet. 1998;351:1763–7.
Edlow BL, Wu O. Advanced neuroimaging in traumatic brain injury. Semin Neurol. 2012;32:374–400.
Barzo P, Marmarou A, Fatouros P, et al. Contribution of vasogenic and cellular edema to traumatic brain swelling measured by diffusion-weighted imaging. J Neurosurg. 1997;87:900–7.
Huisman TA, Schwamm LH, Schaefer PW, et al. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR Am J Neuroradiol. 2004;25:370–6.
Liu AY, Maldjian JA, Bagley LJ, et al. Traumatic brain injury: diffusion-weighted MR imaging findings. AJNR Am J Neuroradiol. 1999;20:1636–41.
Betz J, Zhuo J, Roy A, et al. Prognostic value of diffusion tensor imaging parameters in severe traumatic brain injury. J Neurotrauma. 2012;29:1292–305.
Kidwell CS, Alger JR, Saver JL. Beyond mismatch: evolving paradigms in imaging the ischemic penumbra with multimodal magnetic resonance imaging. Stroke. 2003;34:2729–35.
Wu O, Sorensen AG, Benner T, et al. Comatose patients with cardiac arrest: predicting clinical outcome with diffusion-weighted MR imaging. Radiology. 2009;252:173–81.
Wijman CA, Mlynash M, Caulfield AF, et al. Prognostic value of brain diffusion-weighted imaging after cardiac arrest. Ann Neurol. 2009;65:394–402.
Nakahara M, Ericson K, Bellander BM. Diffusion-weighted MR and apparent diffusion coefficient in the evaluation of severe brain injury. Acta Radiol. 2001;42:365–9.
Scheid R, Preul C, Gruber O, et al. Diffuse axonal injury associated with chronic traumatic brain injury: evidence from T2*-weighted gradient-echo imaging at 3T. AJNR Am J Neuroradiol. 2003;24:1049–56.
Yanagawa Y, Tsushima Y, Tokumaru A, et al. A quantitative analysis of head injury using T2*-weighted gradient-echo imaging. J Trauma. 2000;49:272–7.
Hinson HE, Sheth KN. Manifestations of the hyperadrenergic state after acute brain injury. Curr Opin Crit Care. 2012;18:139–45.
Stuss DT, Binns MA, Carruth FG, et al. The acute period of recovery from traumatic brain injury: posttraumatic amnesia or posttraumatic confusional state? J Neurosurg. 1999;90:635–43.
Rappaport M, Hall KM, Hopkins K, et al. Disability rating scale for severe head trauma: coma to community. Arch Phys Med Rehabil. 1982;63:118–23.
Hall K, Cope DN, Rappaport M. Glasgow Outcome Scale and Disability Rating Scale: comparative usefulness in following recovery in traumatic head injury. Arch Phys Med Rehabil. 1985;66:35–7.
Hammond FM, Grattan KD, Sasser H, et al. Long-term recovery course after traumatic brain injury: a comparison of the functional independence measure and disability rating scale. J Head Trauma Rehabil. 2001;16:318–29.
Reese TG, Heid O, Weisskoff RM, Wedeen VJ. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med. 2003;49:177–82.
Sidaros A, Engberg AW, Sidaros K, et al. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain. 2008;131:559–72.
Kumar R, Gupta RK, Husain M, et al. Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric tests. Brain Inj. 2009;23:675–85.
Rutgers DR, Fillard P, Paradot G, et al. Diffusion tensor imaging characteristics of the corpus callosum in mild, moderate, and severe traumatic brain injury. AJNR Am J Neuroradiol. 2008;29:1730–5.
Fernandez-Espejo D, Bekinschtein T, Monti MM, et al. Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. Neuroimage. 2011;54:103–12.
Smith SM, Jenkinson M, Woolrich MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):S208–19.
Parvizi J, Damasio AR. Neuroanatomical correlates of brainstem coma. Brain. 2003;126:1524–36.
Parvizi J, Damasio A. Consciousness and the brainstem. Cognition. 2001;79:135–60.
Edlow BL, Takahashi E, Wu O, et al. Neuroanatomic connectivity of the human ascending arousal system critical to consciousness and its disorders. J Neuropathol Exp Neurol. 2012;71:531–46.
Schlaug G, Siewert B, Benfield A, et al. Time course of the apparent diffusion coefficient (ADC) abnormality in human stroke. Neurology. 1997;49:113–9.
Grandin C, Hermoye L, Duprez T, et al. Is there an ADC threshold predicting irreversible infarction in hyperacute stroke? J Neuroradiol. 2002;29:68–71.
Sorensen AG, Wu O, Copen WA, et al. Human acute cerebral ischemia: detection of changes in water diffusion anisotropy by using MR imaging. Radiology. 1999;212:785–92.
Kraus MF, Susmaras T, Caughlin BP, et al. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain. 2007;130:2508–19.
Kumar R, Husain M, Gupta RK, et al. Serial changes in the white matter diffusion tensor imaging metrics in moderate traumatic brain injury and correlation with neuro-cognitive function. J Neurotrauma. 2009;26:481–95.
Tovar-Moll F, Evangelou IE, Chiu AW, et al. Thalamic involvement and its impact on clinical disability in patients with multiple sclerosis: a diffusion tensor imaging study at 3 T. AJNR Am J Neuroradiol. 2009;30:1380–6.
Schaefer PW, Huisman TA, Sorensen AG, et al. Diffusion-weighted MR imaging in closed head injury: high correlation with initial Glasgow Coma Scale score and score on modified Rankin scale at discharge. Radiology. 2004;233:58–66.
Zheng WB, Liu GR, Li LP, Wu RH. Prediction of recovery from a post-traumatic coma state by diffusion-weighted imaging (DWI) in patients with diffuse axonal injury. Neuroradiology. 2007;49:271–9.
Galanaud D, Perlbarg V, Gupta R, et al. Assessment of white matter injury and outcome in severe brain trauma: a prospective multicenter cohort. Anesthesiology. 2012;117:1300–10.
Muccio CF, De Simone M, Esposito G, et al. Reversible post-traumatic bilateral extensive restricted diffusion of the Brain A case study and review of the literature. Brain Inj. 2009;23:466–72.
Takayama H, Kobayashi M, Sugishita M, Mihara B. Diffusion-weighted imaging demonstrates transient cytotoxic edema involving the corpus callosum in a patient with diffuse brain injury. Clin Neurol Neurosurg. 2000;102:135–9.
Greer D, Scripko P, Bartscher J, et al. Serial MRI changes in comatose cardiac arrest patients. Neurocrit Care. 2011;14:61–7.
Greer DM. Mechanisms of injury in hypoxic-ischemic encephalopathy: implications to therapy. Semin Neurol. 2006;26:373–9.
Gray FD Jr, Horner GJ. Survival following extreme hypoxemia. JAMA. 1970;211:1815–7.
Schwamm LH, Koroshetz WJ, Sorensen AG, et al. Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging. Stroke. 1998;29:2268–76.
Maxwell WL, Povlishock JT, Graham DL. A mechanistic analysis of nondisruptive axonal injury: a review. J Neurotrauma. 1997;14:419–40.
Povlishock JT, Katz DI. Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehabil. 2005;20:76–94.
Mlynash M, Campbell DM, Leproust EM, et al. Temporal and spatial profile of brain diffusion-weighted MRI after cardiac arrest. Stroke. 2010;41:1665–72.
Kinney HC, Korein J, Panigrahy A, et al. Neuropathological findings in the brain of Karen Ann Quinlan. The role of the thalamus in the persistent vegetative state. N Engl J Med. 1994;330:1469–75.
Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain. 2000;123:1327–38.
Tong KA, Ashwal S, Holshouser BA, et al. Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol. 2004;56:36–50.
Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8:165–74.
Melhem ER, Itoh R, Jones L, Barker PB. Diffusion tensor MR imaging of the brain: effect of diffusion weighting on trace and anisotropy measurements. AJNR Am J Neuroradiol. 2000;21:1813–20.
Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med. 2004;51:807–15.
Marino S, Zei E, Battaglini M, et al. Acute metabolic brain changes following traumatic brain injury and their relevance to clinical severity and outcome. J Neurol Neurosurg Psychiatry. 2007;78:501–7.
We are grateful to the patient and his family for participating in this study and for sharing their photos and videos. All photos and videos are shown with consent. We thank Kristin Parlman and Anne McGrail for their assistance with functional outcome assessments. We also thank the nurses and the physical, occupational, and speech/language therapy teams at Massachusetts General Hospital, Spaulding Rehabilitation Hospital, and Crotched Mountain Rehabilitation Center. We thank Kathryn R. Tringale and Brittany Sorice for assistance with video capture and editing. We are grateful to Dr. Hannah C. Kinney for consultation regarding neuroanatomic localization of the regions of interest used in this study.
This study was supported in part by grants from the National Institutes of Health (R25NS065743 and P41EB015896), the National Institute on Disability and Rehabilitation Research (H133A120085), and the Center for Integration of Medicine and Innovative Technology (Boston, MA). The views in this article represent those of the authors alone, and do not necessarily represent the views of the Department of Veterans Affairs or the U.S. Government.
Conflict of interest
Brian L. Edlow and Joseph T. Giacino contributed equally to this article.
Ona Wu and Leigh R. Hochberg contributed equally to this article.
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Edlow, B.L., Giacino, J.T., Hirschberg, R.E. et al. Unexpected Recovery of Function After Severe Traumatic Brain Injury: The Limits of Early Neuroimaging-Based Outcome Prediction. Neurocrit Care 19, 364–375 (2013). https://doi.org/10.1007/s12028-013-9870-x
- Traumatic brain injury
- Magnetic resonance imaging
- Traumatic axonal injury
- Diffusion-weighted imaging
- Apparent diffusion coefficient
- Diffusion tensor imaging